Combinatorial and cross-fiber averaging transform muscle electrical responses with a large stochastic component into deterministic contractions.

Pyloric muscles of the stomatogastric neuromuscular system of the lobster Panulirus interruptus produce highly deterministic (range, less than +/- 6% of mean amplitude) contractions in response to motor nerve stimulation with unchanging spike bursts containing physiological (5-10) spike numbers. Intracellular recordings of extrajunctional potentials (EJPs) evoked in these muscles by motor nerve stimulation revealed a large, apparently stochastic amplitude variation (range, +/- 36% of mean amplitude). These observations raised the question of how do electrical responses with a large amplitude variation give rise to deterministic muscle output? We show here that this question is likely resolved by (1) combinatorial averaging within individual muscle fibers of the multiple EJPs that occur in motor neuron bursts, and (2) averaging across muscle fibers whose electrical responses are uncorrelated. Synapses with high inherent variability are also present in vertebrate CNSs. Combinatorial averaging in multispike inputs would also reduce variation in postsynaptic response at these synapses. The data reported here provide further support that bursting presynaptic activity could make such synapses functionally deterministic as well.